Evolutionary biology has a punctuated history. It arose as a
conceptual macromutation on November 24, 1859 -- "disgorged,"
as Mencken (1931) put it, "in one stupendous and appalling
dose" -- and has undergone stasis or slow anagenesis ever since.
Indeed, much of the field still consists of repeated demonstrations of
phenomena first described by Darwin, or of epiphenomena derived from
them.

The study of speciation, however, is a conspicuous exception. Despite
the title of his famous book, Darwin was notably unsuccessful in solving
the real problem of organic diversity: why plants and animals in a
habitat fall into discrete, nonoverlapping packages. It is widely
accepted that his failure came from his inability to conceptualize
species as noninterbreeding groups (see Mayr 1959) and to recognize that
the origin of species was identical to the origin of the barriers to
interbreeding. Because Darwin considered species to be only highly
evolved morphological varieties (indeed, The Origin of Species should
have been called The Origin of Adaptations), he confused adaptation
within lineages with the origin of new lineages. Although the two are
connected, the former does not automatically produce the latter.
Understanding how one species of warbler becomes adapted to its habitat
does not explain why four other distinct species -- and no intermediates
-- occupy the same patch of forest.

One solution was suggested by geneticists like Bateson and
Goldschmidt, who correctly conceived the species problem to be the
explanation of organic gaps, but then mistakenly ascribed them to single
mutations causing large morphological change. This idea foundered on the
lack of a convincing scenario for fixing these mutations and on the
evidence that species differed in not one but many genes. For many years
after Darwin, the origin of species remained the most important unsolved
problem of evolution.

The mathematical evolutionists of the modern synthesis had little to
say about this problem, and much of what they did say was wrong. Our
modern theories of speciation derive almost entirely from a naturalist
and an experimentalist, Ernst Mayr and Theodosius Dobzhansky, and their
two classic books, Genetics and Origin of Species (Dobzhansky 1937) and
Systematics and the Origin of Species (Mayr 1942), later rewritten and
expanded as Animal Species and Evolution (Mayr 1963).

On the occasion of Mayr's ninetieth birthday, I am pleased to
pay him tribute by discussing and evaluating his four major
contributions to the species problem. Three of these -- the emphasis on
discontinuous organic forms, the encapsulation of such discontinuities
in the "biological species concept," and the theory of
allopatric speciation -- are milestones of evolutionary biology that
constitute the modern dogma of speciation. Mayr's fourth
contribution, the idea of "genetic revolutions" in isolated
populations, is decidedly less important, and, it seems to me, probably
incorrect. It will be impossible to discuss Mayr's work without
also mentioning that of Dobzhansky, whose genetic expertise made the
theory of speciation a true product of the modern synthesis.

ORGANIC DISCONTINUITIES

Many field naturalists find it hard to doubt that organisms in any
habitat fall into discrete groups, which have a reality not shared by
higher levels of classification like genera and families. The idea of
organic discontinuity has a long tradition, beginning with
Linnaeus' classification, and was recognized by even Darwin in The
Descent of Man (1871): "Independently of blending from
intercrossing, the complete absence, in a well-investigated region, of
varieties linking together any two closely-allied forms, is probably the
most important of all the criteria of their specific distinctness"
(1871, p. 215).

Nevertheless, some biologists contend that these discontinuities are
purely subjective artifacts of human perception. One such dissenter was,
surprisingly, J. B. S. Haldane, who observed that "the concept of a
species is a concession to our linguistic habits and neurological
mechanisms . . . a dispute as to the validity of a specific distinction
is primarily a linguistic rather than a biological dispute" (1956,
p. 96). The idea that species are not real is particularly popular with
systematists (e.g., Sokal and Crovello 1970; Mishler and Donoghue 1982;
Nelson 1989) and botanists (e.g., Raven 1976; Levin 1979), who emphasize
the lack of easily recognized species in plants. Those entertaining this
view, of course, require no theory of speciation beyond that given by
Darwin.

The recognition of the reality of species is the key to explaining
organic diversity, and it was largely Mayr and Dobzhansky who impressed
this reality upon evolutionists: "Only after the naturalists had
insisted on the sharp definition of local species was there a problem of
bridging the gap between species. And only then did the problem arise
whether or not the species is a unit of evolution, and what sort of
unit" (Mayr 1963, p. 30). The emphasis here is on
"local," for, as Mayr noted, these discontinuities are most
evident in sympatric groups, and largely disappear under the inclusion
of geographic populations. This disparity between local and isolated
populations was a major inspiration for his theory of allopatric
speciation.

Mayr discussed the reality of species at length in his first major
paper on speciation (1940), supporting the idea with evidence from bird
taxonomy, and produced a longer discussion in chapter 7 of Systematics
and the Origin of Species. Dobzhansky, on the other hand, solved the
problem by fiat at the very beginning of Genetics and the Origin of
Species: "Discrete groups are encountered among animals as well as
plants, in those that are structurally simple as well as in those that
are very complex. Formation of discrete groups is so nearly universal
that it must be regarded as a fundamental characteristic of organic
diversity." (1940, p. 5.)

Given the importance of the problem and the vocal minority of
critics, it is surprising that there are few studies of the reality of
species in a single locality. Existing work falls into two categories.
The first notes the remarkable concordance between species described by
Western taxonomists and the "kinds" recognized by indigenous
peoples. Such concordance has been demonstrated for both plants (Berlin
1992) and birds (Mayr 1963; Diamond 1966), although the geographic
sampling is limited.

This evidence has not convinced everyone. In response, Ridley noted,
"However, the fact that independently observing humans see much the
same species in nature does not show that species are real rather than
nominal categories. The most it shows is that all human brains are wired
up with a similar perceptual cluster statistic." (1993, p. 404.)
His criticism, echoing that of Haldane, fails to recognize that all
scientific progress comes from the agreement of independent observers.
(Is the distinction between chemical elements, for example, an artifact
of the way our brains are wired to perceive matter?) If nothing else,
these congruent classifications give strong evidence that species are
real, although they do not prove them more real than other categories of
classification. One could test this last idea by asking nonbiologists to
place all local organisms into seven hierarchical categories, and then
comparing the result to traditional Western taxonomy. (I would bet a
substantial sum that the congruence seen for species would largely
vanish at higher levels.)

Perhaps a more convincing approach would involve cluster analysis of
either genetic or morphological diversity within one area. Although such
analyses are themselves designed to separate groups, they cannot create
such groups when they do not exist. There are many multivariate analyses
of both morphological and genetic variation showing fairly distinct
differences among sympatric groups (e.g., Grant 1957; Neff and Smith
1978; Humphries et al. 1981; Futuyma 1991). These investigations,
however, are often performed on species already known to differ
morphologically and are usually limited to two groups. One would like to
see such analyses performed on every individual bird or plant within one
habitat. Mayr himself (1992b) conducted a valiant though nonstatistical
study of this kind, concluding that 90.8% of the plant species in
Concord, Massachusetts were clearly delimited.

My own opinion vacillates between Dobzhansky's view that the
reality of species is evident to any reasonable person, and a wish that
someone would settle the issue through detailed study of at least a few
sympatric groups. (I cannot imagine, however, that funding agencies
would rush to support this work). Such studies would be particularly
useful in plants, in view of botanists' repeated claims that plant
"species," such as oaks, often form intergrading, hybridizing
units. It is entirely possible that many such "species
complexes" are actually ecotypes of a single species,
differentiated in only a few characters by intense habitat selection
(Coyne et al. 1988).

A major unsolved question about the reality of species is whether
discrete groups also occur in asexually reproducing taxa. The answer
would have major implications for understanding why organic forms are
discontinuous, particularly in estimating the relative contributions of
sexual reproduction versus discrete ecological niches. Only a few
studies of eukaryotes have addressed this problem. Holman (1987)
concluded that asexually reproducing groups of bdelloid rotifers were
actually recognized more consistently than their sexually reproducing
relatives. This conclusion, however, was based not on morphology or
genetics, but on stability of nomenclature through successive taxonomic
revisions. Analyzing mosses of the genus Tortula, Mishler (1990) found
no difference in the amount of morphological variation among populations
of two sexual versus two asexual "species," although he
examined only 10 or 20 individuals per species. There is a clear need
for much more work of this kind, using phenetic and not systematic
criteria.

THE BIOLOGICAL SPECIES CONCEPT

The recognition that discrete groups exist in one location
immediately demands a definition, or rather a concept that encapsulates
these groups in words. Although morphological species concepts were
dominant until the 1930s, some biologists, such as Karl Jordan,
suggested criteria based on interbreeding (for a summary of this early
work, see Mayr 1942, 1957, 1982). However, it was Dobzhansky and
especially Mayr who provided the definitive rejection of phenetic
concepts, replacing them with what has become known as the
"biological species concept," or BSC. In later publications,
Mayr (1963, 1982) slightly revised the BSC, emphasizing that it is best
applied to sympatric taxa. This removed the problematic words
"potentially interbreeding" from his definition, although
allopatric taxa that produce sterile or inviable hybrids in captivity
are surely biological species.

Because the observation of discrete sympatric groups almost
immediately suggests a species concept based on interbreeding and its
absence, it is surprising that such a view did not become popular until
about 1940. Perhaps this idea occurs most readily to the geneticist,
explaining why the first explicit version of the BSC came from
Dobzhansky. As he explained, "Any discussion of these problems
should have as its logical starting point a consideration of the fact
that no discrete groups of organisms differing in more than a single
gene can maintain their identity unless they are prevented from
interbreeding with other groups. . . . Hence, the existence of discrete
groups of any size constitutes evidence that some mechanisms prevent
their interbreeding, and thus isolate them" (Dobzhansky 1935, p.
281).

Mayr, of course, gets the credit for refining, popularizing,
defending, and working out the consequences of the BSC in his numerous
writings on species concepts. Besides the original definition,
Dobzhansky's major contribution to this notion is his
classification of the biological factors preventing hybridization, the
so-called "reproductive isolating mechanisms," and their
division into categories acting before (prezygotic) and after
(postzygotic) fertilization. A major portion of Genetics and the Origin
of Species is devoted to describing and illustrating these mechanisms.

The BSC has become the dominant evolutionary view of species for at
least three reasons. First, it is able to handle problems that cannot be
solved by phenetic concepts, such as morphologically identical species,
polymorphism, sexual dimorphism, and phenotypically different stages of
the life cycle. Second, it shows that the species is an evolutionary
unit in that it delimits the spread of a generally advantageous allele,
such as one raising fecundity by 0.2%. In this sense, the species is the
entity that evolves, and hence the locus of micro- and macroevolutionary
change (see Gould 1994). Finally, and most important, it provides a
research program for understanding the genesis of biological diversity:
The origin of species is now seen as the origin of reproductive
isolating mechanisms. The problem then translates immediately to
understanding the evolution of factors like microhabitat preference,
mate discrimination, and hybrid sterility. It is a testament to the
power of the BSC that virtually everyone studying the origin of species
concentrates on reproductive isolating mechanisms.

The BSC has nevertheless encountered severe opposition, usually from
systematists, and many alternative concepts have been proposed. Table l
gives only a sample of the more recent ones, and each year brings new
contenders. Moreover, there is a disturbingly large literature filled
with acerbic attacks and defenses of all of these concepts (for recent
examples, see Coyne et al. 1988; Masters and Spencer 1989; Otte and
Endler 1989; Ereshefsky 1992; Mayr 1992b); much of this argument leaves
the solid ground of biology for the marshy hinterlands of philosophy.

No alternative concept, however, has displaced the BSC among
evolutionists, although systematists seem increasingly to embrace
typological views in which species are defined as possessing one or more
diagnostic or apomorphic features (so-called "phylogenetic species
concept"). I believe that the failure of alternative concepts comes
largely from their inability to offer an entree into the problem of
biological diversity and to inspire interesting new research. The
evolutionary and phylogenetic concepts, for example, distinguish species
by phenotypic difference -- and would split every morphologically
diagnosable population into a new species -- but suggest no program for
understanding the coexistence of phenotypically distinct but related
species. Proponents of the recognition concept maintain that it is not
"relational"; that is, species are not detected or defined by
their reproductive isolation from one another (Paterson 1985). It thus
offers no way to study the evolution of mating discrimination among
species. The ecological species concept may be an exception, as the
discreteness of species could be ascribed to the discreteness of niches.
It is not clear, however, whether niches really are discrete, and, at
any rate, the concept is impossible to use given the difficulty of
categorizing "minimally different adaptive zones." Mayr
(1992b) noted that many systematists proposing alternative species
concepts actually revert to the BSC when dealing with problems like
sibling species.

I have no idea why the BSC, which despite its difficulties has
inspired so much valuable research, also seems to ignite so much
controversy, nor why many biologists are intent on replacing it with
concepts even more problematic. Some systematists apparently fear that
acceptance of the BSC will trivialize their research program. For
example, "The militant view that systematists need to embrace is
that the responsibility for species concepts lies solely with
systematists. If we continue to bow to the study of process over
pattern, then our endeavors to elucidate pattern become irrelevant"
(Wheeler and Nixon 1990, p. 79). It is clear, however, that the many
pages of argument have not increased our understanding of evolution, and
that the best advice may be that proffered half a century ago by the
prescient Hogben (1940): "We need not prolong a barren controversy
about the various definitions of species."

Accepting that species do exist and correspond to interbreeding
groups separated by reproductive gaps, one may still wonder what feature
of organisms inevitably produces these gaps. Why aren't there just
a few extremely variable species? This is one of the most important and
least considered questions of speciation. Mayr and Dobzhansky both had
answers, but they verged on the teleological, implying that nature
somehow engineers these gaps to protect adaptive gene complexes:
"Hence maintenance of life is possible only if the gene patterns
whose coherence is tested by natural selection are prevented from
disintegration due to unlimited hybridization. It follows that there
must exist discrete groups of forms, species, which consist of
individuals breeding inter se, but prevented from interbreeding with
individuals belonging to other groups of similar nature."
(Dobzhansky 1937, p. 405.)

"The division of the total genetic variability of nature into
discrete packages, the so-called species, which are separated from each
other by reproductive barriers, prevents the production of too great a
number of disharmonious incompatible gene combinations. This is the
basic biological meaning of species, and this is the reason why there
are discontinuities between sympatric species." (Mayr 1969, p.
316.)

These explanations, probably influenced by Sewall Wright's
concept of the adaptive landscape, do not rest on the firm populational
thinking so important in the other writings of Mayr and Dobzhansky, nor
do they square with the notion that some isolating mechanisms, such as
hybrid sterility, cannot be the direct target of natural selection.
There is still no good explanation for the ubiquity of organic gaps. The
solution may involve pleiotropy, trade-offs, and sexual reproduction
(adapting to one environment reduces fitness in others, causing problems
in hybrids), the discreteness of ecological niches (there is a limit to
the similarity of competing forms), or a combination of these factors.
Several theoretical studies (Rosenzweig 1978; Hopf and Hopf 1985; Brown
and Vincent 1992) have suggested that ecological factors alone can
create phenotypic gaps between taxa, but the answer is not yet clear.
Observing whether asexually reproducing taxa fall into discrete groups
will go a long way toward solving the problem.

ALLOPATRIC SPECIATION

Mayr's explanation for the origin of biological species was
allopatric speciation: geographically isolated populations of a single
species evolve reproductive isolating mechanisms that later allow them
to coexist in sympatry. To describe Mayr's multifarious evidence
for this process would deprive the student of the great joy of reading
chapter 7 of Systematics and the Origin of Species, an experience that
turned many of us toward the study of speciation. The exhaustive
biogeographic evidence given in this chapter reminds one strongly of The
Origin of Species and immediately convinced most evolutionists of the
importance of allopatric speciation. The novelty of Mayr's argument
was the explanation of reproductive gaps as the incidental byproduct of
evolutionary divergence between isolated populations, gaps that can only
be seen when the newly evolved species become sympatric. With this
argument, organic diversity had at last received a convincing
explanation.

Dobzhansky contributed to this theory by summarizing the genetic
evidence for the importance of geographic isolation. In a famous
five-page discussion in Genetics and the Origin of Species (1937, pp.
254-258), he refuted the notion that speciation results from single
mutations, demonstrating that most forms of reproductive isolation
involve epistatic interaction between alleles fixed in different demes.
If an ancestral population has the two-locus genotype aabb, one isolated
population might evolve to aaBB and another to AAbb. If individuals
carrying the A allele are sexually isolated from the carriers of B, or
the hybrid genotype A_B_is sterile or inviable, reproductive isolation
would be a pleiotropic by-product of purely adaptive evolution.
Dobzhansky concluded that geographic isolation is required for
speciation, as the incompatibility between A and B alleles segregating
in one population would prevent the evolution of linkage disequilibrium
between the epistatically acting loci. This deductive argument for
allopatry nicely complements the inductive biogeographic arguments of
Mayr. (One cannot discuss Dobzhansky's contribution without at
least mentioning that of H. J. Muller, who, in two brilliant but obscure
papers [1940, 1942], expanded Dobzhansky's discussion, illustrating
it with examples from his own work on Drosophila). The value of the
genetic argument is the demonstration that reproductive isolation, an
adaptive valley between populations, evolves incidentally while each
population is scaling an adaptive peak. There is thus no need to embrace
the common misconception that speciation involves loss of fitness within
a population.

An important difference between Mayr and Dobzhansky was their
appraisal of reinforcement, the idea that natural selection can directly
increase reproductive isolation between two incipient species that
become sympatric. Dobzhansky held that if some hybrid sterility or
inviability evolved in allopatry, natural selection in subsequent
sympatry would favor mating discrimination, increasing the frequency of
alleles preventing maladaptive hybridization. Reinforcement could then
complete speciation by reducing gene flow to zero. To the end of his
life, Dobzhansky believed that this process was part of nearly every
speciation event, a belief that sometimes forced him into awkward
positions. In 1940, for example, he floated the idea that an island
invader might become a new species only when its ancestor invaded a
second time, providing the selective pressure to finish the job.
Dobzhansky's influence led to the widespread acceptance of
reinforcement, which was widely taught (as I learned it) to be the final
step in speciation. We now know that much of the approbation was
uncritical: theory shows that reinforcement is difficult to achieve, and
much of the supporting data from natural were ambiguous or wrongly
interpreted (see, e.g., Butlin 1987; Spencer et al. 1987; Rice and
Hostert 1993). Although there is still suggestive evidence for
reinforcement (Coyne and Orr 1989), it will take years of work to
determine whether it is common.

Mayr has been far less enthusiastic about reinforcement, maintaining
instead that most reproductive isolation is an accidental byproduct of
genetic divergence in allopatry: "The question is, however, whether
or not this [reinforcement] is the only way by which reproductive
isolation can be established. Naturalists, from von Buch down to our
contemporaries, have always believed that good species can complete
their development in isolation. They find an abundance of cases in
nature which seem to permit no other interpretation. The most conclusive
evidence is, of course, presented by the multiple invasion of islands by
separate colonizing waves coming from the same parental stock."
(Mayr 1942, p. 157; see also Mayr 1959, 1963.)

Mayr's insistence on the primacy of allopatric speciation was
accompanied by his famous critiques of sympatric speciation, beginning
with chapter 8 of Systematics and the Origin of Species, continuing in
his first paper in Evolution (Mayr 1947), and culminating in chapter 15
of Animal Species and Evolution. These analyses, inspired by the
widespread idea that reproductive isolation could easily evolve in the
presence of gene flow, focused on both theoretical models, all of which
Mayr diagnosed with "fatal flaws," and the biogeographic data,
which Mayr thought more parsimoniously interpreted as favoring
allopatric speciation.

With the possible exception of the founder-effect theory, no aspect
of Mayr's work has caused more controversy, or motivated more
research, than his criticism of sympatric speciation. Entire books, such
as M. J. D. White's Modes of Speciation (1978), were written to
counter Mayr's arguments, these rebuttals often suffused with anger
at Mayr's supposed dogmatism. The controversy also inspired a body
of theoretical work, beginning with the paper of Maynard Smith (1966)
and summarized recently by Rice and Hostert (1993). While confirming
that sympatric speciation is more difficult to achieve than the
allopatric alternative, newer theories do not support Mayr's belief
that speciation nearly always requires the absence of interbreeding.
Moreover, recent laboratory experiments, particularly those of Rice and
Salt (1990), have achieved a surprising amount of reproductive isolation
in the presence of gene flow, though it is arguable whether they are
realistic models of nature. Sympatric speciation hence cannot be
questioned as a theoretical possibility, at least not with the vigor
shown by Mayr. (It is a mistake, however, to think that Mayr completely
ruled out sympatric speciation. On several occasions [e.g., 1976, p.
144; 1982, p. 605; 1988, p. 376], he noted that it might not be rare in
host-specific insects.)

The most important task for supporters of sympatric speciation,
however, is to demonstrate that it occurs in nature. Although allopatric
speciation can be confirmed from the biogeographic evidence adduced in
Systematics and the Origin of Species, the same is not true for
sympatric speciation, which also requires historical observation or
measurements of gene flow. This has been achieved in allopolyploid
species of Tragopogon (Novak et al. 1991; Soltis and Soltis 1991), and
it is almost certain that allopolyploidy is a frequent cause of
sympatric speciation in plants. But, despite ardent debate, there is
still only one reasonable candidate for the sympatric evolution of
reproductive isolation in animals: the host races of Rhagoletis
pomonella (Feder et al. 1988). Even these races, however, have not
become full species.

The only fairly convincing evidence I can imagine, save actually
witnessing sympatric speciation, is finding sister species of highly
mobile organisms on small and remote oceanic islands. The discovery of
two sister species of Geospiza on Cocos Island, the most isolated of the
Galapagos, would be hard to explain by any sort of allopatric
speciation. Cocos, alas, harbors only one species of finch. As far as I
know, there have been no thorough studies of this problem, although data
for such an analysis surely exist. A recent study of monophyletic
cichlid groups in two small African crater lakes (Schliewen et al.
1994), which are aquatic islands, strongly suggests the possibility of
sympatric speciation. White (1978) argued that adaptive radiations of
wingless insects on oceanic islands prove sympatric speciation. The
weakness of this argument is that such sedentary creatures might
speciate allopatrically in a very small area.

It is possible that, except for allopolyploid plants, we will never
know how often sympatric speciation occurs in nature. It is clearly more
difficult to achieve sympatric than allopatric reproductive isolation,
but perhaps the ecological opportunity for the former is far more
frequent. (Can geographic isolation really account for our millions of
species?) We are thus faced with an epistemological problem, leading to
Mayr's (1963, p. 480) conclusion that "the burden of proof
rests, however, on supporters of this alternative mode of
speciation." This burden will only be eased when we find ways to
distinguish sympatric from allopatric speciation in nature.

FOUNDER-EFFECT SPECIATION

Although the three ideas discussed above were highly salubrious, I
regret that the same cannot be said of Mayr's theory of
founder-effect speciation, which has infected evolutionary biology with
a plague of problematic work.

According to Mayr, this theory had two sources: "One was the
observation that aberrant populations of species almost invariably are
peripherally isolated and that, more often than not, the most aberrant
population is the most distant one. . . . By contrast, the amount of
geographic variation in contiguous species ranges is usually minor. The
other reason, pointed out by Haldane (1937, 1957) is that large,
widespread populations -- in fact all more populous species -- are
evolutionarily inert, because new alleles, even favorable ones, require
very long periods of time to spread throughout the entire species
range." (1982, p. 604.)

The geographic patterns were first described, without an explanatory
theory, in Systematics and the Origin of Species. The theory appeared in
1954, and was discussed at length in Animal Species and Evolution.
Mayr's basic idea is that genetic drift and epistasis play a key
roles in the speciation of small, colonizing populations. This drift
would supposedly cause genome-wide homozygosity, imposing novel
selective pressures on alleles originally selected on heterozygous
genetic backgrounds. This would in turn set off a "genetic
revolution," producing large changes in the frequencies of
still-segregating alleles, and establishing new polymorphic
"balanced systems" when the colonizing population increased in
size. The genetic divergence between ancestor and descendant was said to
cause not only reproductive isolation, but also profound morphological
change not achievable by conventional Darwinian selection: "The
genetic reorganization of peripherally isolated populations, on the
other hand, does permit evolutionary changes that are many times more
rapid than the changes within populations that are part of a continuous
system. Here then is a mechanism which would permit the rapid emergence
of macroevolutionary novelties without any conflict with the observed
facts of genetics" (Mayr 1954, p. 176).

The influence of this theory has been profound. It spawned several
similar theories with confusing names, including founder-flush
speciation, flush-founder speciation, flush-crash speciation, and
genetic transilience. The subtle differences among these theories were
described by Carson and Templeton (1984) and Provine (1989). Their
common elements are the colonization of an empty habitat by a few
individuals, followed by expansion (and sometimes crashes) of population
size, and the existence of epistasis, genetic drift, and maladaptive
evolution within the colonizing population. These theories have, in
turn, buttressed the claim of punctuated equilibrium that nonadaptive
gene frequency change in peripheral populations is an important part of
speciation and morphological change, helping explain the sudden
appearance of evolutionary novelties. (This claim, however, has
apparently been jettisoned by its proponents, who now suggest that a
punctuated fossil record may result from conventional natural selection
after all [Gould and Eldredge 1993]). Finally, founder-effect theories
have inspired a number of laboratory experiments examining the
connection between founder events and reproductive isolation.

These theories and experiments have encountered strenuous objections,
usually from population geneticists. Mayr's observation that
isolated populations are morphologically deviant can, for example, be
explained by the more parsimonious theory that isolated populations
experience strong selection in a novel environment, with speciation a
byproduct of adaptive change. This is the classic tale of adaptive
radiation, once the favored explanation for luxuriant and rapid
speciation on islands (Coyne 1993). Moreover, there is no evidence that
proposed examples of founder-effect speciation, such as the Hawaiian
Drosophila, have experienced strong genetic drift (they have ample
genetic polymorphism), nor any reason to suppose that they are not
simply examples of adaptive radiation like the Galapagos finches or New
Guinea birds of paradise.

Mayr criticized the adaptive-divergence explanation by claiming that
the environment of many aberrant island populations was nearly identical
to that of their more widespread relatives. The evidence for such
identity, however, consisted of only two observations. Mayr noted that
the islands around New Guinea, which harbor divergent populations of
birds, "lie in the same climatic district as the nearest part of
the mainland of New Guinea" (1954, p. 158). Referring to the
divergent species of Tanysiptera on Numfor Island, he further observed
that "The climate of Numfor is much like that of the opposite coast
of New Guinea, thus the selection-pressure by the physical environment
will remain much as it was in the previous range. The flora is somewhat
different and the fauna is somewhat impoverished, but the only
potentially serious predator, Accipiter novaehollandiae, occurs both on
Numfor and New Guinea. The physical and biotic environments are rather
similar in both places." (1954, p. 168.) These observations provide
a rather shaky foundation for a new theory of speciation! Even very
similar environments, moreover, can select for dissimilar phenotypes if
gene flow is completely absent. This is particularly true of sexual
selection, which seems to be involved in many adaptive radiations.

The theoretical basis of founder-effect speciation has also been
questioned, as all of the models are verbal, lacking a convincing
mathematical demonstration that founder events can produce full
reproductive isolation with reasonable probability (Lande 1980;
Charlesworth et al. 1982; Barton and Charlesworth 1984). The supposed
evolutionary inertness of large populations, an argument also used by
Wright (1931) to support his shifting-balance theory, is based on no
evidence save Haldane's calculation that one cannot impose strong
selection on many characters at once. This cost-of-selection argument,
however, does not prove that large populations cannot evolve, only that
no population can evolve too quickly. There is still no theoretical
reason to claim that mass selection is unable to produce evolutionary
novelties.

Reviewing the laboratory studies of founder events, Rice and Hostert
(1993), concluded that some experiments produced small amounts of
reproductive isolation, but that this isolation did not necessarily
require genetic drift. More important, repeated foundings and flushings
have failed to yield even moderate reproductive isolation, casting doubt
on the view that the process can quickly produce full species. Although
proponents of founder-effect speciation sometimes argue that it is a
very rare event, Rice and Hostert note that "such a philosophy
makes the model virtually impossible to reject experimentally."

The popularity of founder-effect theories, however, seems curiously
immune to these criticisms. Provine (1989, p. 72) observed -- correctly,
I think -- that "some version of Mayr's founder effect and
genetic revolution has been the favored explanation for at least island
speciation since 1954." Since the mid-1980s, many questions of
speciation, some of them tractable, have been neglected in favor of
seemingly endless debates about this process.

I am not sure why genetic-drift theories of speciation have
outcompeted more conventional Darwinian ideas of adaptive radiation.
Unlike the case of black-body radiation, in which a new observation
could not be explained by existing paradigms of physics, there is no
observation about nature that demands a new theory of speciation. The
popularity of founder-effect theories recalls that of another
complicated and hard-to-test alternative to mass selection,
Wright's shifting-balance theory of evolution. Instead of
considering only natural selection, founder-effect and shifting-balance
theories involve combinations of selection, drift, and population
structure, conjuring up Wright's seductive picture of the adaptive
landscape. The penchant for new and more elaborate theories may stem
from a general malaise provoked by the apprehension that Darwin and
Fisher may have been correct in emphasizing the ubiquity of simple,
garden-variety mass selection. Unlike that of physics, the fundamental
paradigm of evolutionary biology has not changed in over a century, and
it is sometimes depressing to think that we may be forever sweeping up
behind the Darwinian elephant. Dissatisfaction with traditional
Darwinian explanations can be seen in many areas of biology, probably
contributing to the popularity of saltationism in developmental biology,
species selection in paleobiology, and "adaptive mutation" in
molecular biology.

Of course, it is not easy to get conclusive evidence for even the
conventional process of adaptive radiation (do we really understand
speciation in Darwin's finches?), so it would clearly be
inappropriate to reject founder-effect theories out of hand. But until
we find explicit ways to test them against their Darwinian alternative,
the literature will remain filled with inconclusive debate.

CONCLUSION

Reading the works of the modern synthesis, one is struck by how much
clarity was brought to the species problem by Mayr and Dobzhansky, and
how little by their major theoretical colleagues, Fisher, Haldane, and
Wright. Of these three, only Fisher (1930, chap. 6) proposed his own
theory of speciation, an unfortunate model of sympatric or clinal
divergence caused by disruptive selection, with reproductive isolation
completed by reinforcement. Like his adherence to a morphological
species concept, Fisher's view of speciation descended directly
from Darwin, who believed that new species arose to better fill the
niches in a single habitat: "the more diversified the descendants
from any one species become in structure, constitution, and habits, by
so much will they be better enabled to seize on many and widely
diversified places in the polity of nature, and so be enabled to
increase in numbers" (Darwin 1859, p. 112). Fisher explicitly
acknowledged this inheritance by beginning The Genetical Theory of
Natural Selection with a quotation from William Bateson: "As Samuel
Butler so truly said: 'To me it seems that the "Origin of
Variation," whatever it is, is the only true "Origin of
Species."'"

Haldane, as we have seen, was not convinced that species were real,
and in the Causes of Evolution (1932) limited his discussion of
speciation to the genetics of morphological differences between taxa.
Wright, who accepted both the biological species concept and allopatric
speciation quite early, nevertheless largely ignored the issue; his two
papers on speciation (1940a,b) are tendentious arguments for the
shifting-balance theory. His ideas did surface, however, in
founder-effect models of speciation.

Mayr (1992a) ascribed theoreticians' meager contribution to the
species problem to their lack of experience with natural populations and
consequent inability to see that speciation begins as variation among
geographic isolates. I believe, however, that there is another important
reason. During the modern synthesis, the major job of theoretical
population genetics was to provide the mathematical framework for
Darwinism: genetic and phenotypic change within a lineage. Fisher is
best known, of course, for his fundamental theorem of natural selection,
the most famous equation of adaptive change. Even Wright's
shifting-balance theory, which introduced the novelties of genetic drift
and multiple populations, deals essentially with the diffusion of an
adaptation through a single interbreeding unit. When applied to the
problem of speciation, such a program can do no better than suggest that
natural selection directly favors an increase in the number of species
and the size of gaps between them. This led Darwin and Fisher to propose
that species resulted from selection to reduce intraspecific
competition, and may explain the continuing popularity of reinforcement
and sympatric speciation.

Although these processes might occur, they are ancillary to the true
problem of speciation, which simply cannot be framed as a process
occurring within one lineage. The solution requires one to recognize a
phenomenon not encompassed by classical Darwinism: reproductive
isolation. A reproductive isolating mechanism is a composite character
of two species considered together, and, except in cases of
reinforcement, not the direct product of natural selection. (It is hard,
for example, to envision a selective advantage to evolving hybrid
sterility and inviability). It was the genius of Mayr and Dobzhansky to
first recognize that the origin of species was equivalent to the origin
of a genetic interaction, and then to explain its evolution by
conventional Darwinian means. (Perhaps this notion was inspired by their
experience as naturalists, which allowed them to observe the coexistence
of related species.) The success of this whole approach rests, of
course, on adopting the biological species concept. As Mayr observed,
"The word species thus became a word expressing relationship, just
like the word brother, which does not describe any intrinsic
characteristics of an individual but only that of relationship to other
individuals; that is, to other offspring of the same parents. This new
species concept meant a complete change in the ontological status of
species taxa." (1992b, p. 223.)

Under this view, species are merely evolutionary accidents, the
pleiotropic and nonadaptive byproducts of evolutionary change within
lineages. I think that this idea is unpalatable to some, and unable to
replace the belief that natural selection must somehow favor an increase
in organic diversity. Such an adaptationist bent may motivate much of
the opposition to Mayr's theories.

Speciation, then, is an epiphenomenon of Darwinism in only the
trivial sense that, like nearly all evolutionary phenomena, it occurs by
gradual change of populations, usually impelled by natural selection.
But recognizing the importance of reproductive isolation opens up a
whole range of questions beyond the realm of classical Darwinism. I
mention only a few: the ecology and biogeography of polyploid plants
(Soltis and Soltis 1991), the rate of origin of postzygotic isolation
among isolated populations (Coyne and Orr 1989), and the explanation of
the large effect of the X chromosome on hybrid sterility and inviability
(Charlesworth et al. 1987).

Mayr is sometimes criticized for becoming famous by popularizing the
ideas of others, and he readily admitted (1955, 1982) that both the
biological species concept and allopatric speciation were suggested by
earlier workers. (The founder-effect theory, however, is truly original,
as are many other ideas of Mayr; see Futuyma 1994). But this criticism
could also be leveled at Darwin -- after all, evolution was mentioned by
his own grandfather, and natural selection by Patrick Matthew in 1831.
Mayr and Darwin earned their fame for the same reason: each recognized
the importance of earlier suggestions, worked out their consequences in
detail, and showed how they were consistent with the known facts of
biology. When Mayr erred, as I think he did with founder-effect
speciation, his errors were adopted widely; but his successes were far
more numerous and spectacular.

The currency of science is truth, and all biologists are ultimately
valued by their contribution to our understanding of nature. Ernst
Mayr's explanation of the origin of species is surely one of the
greatest achievements of evolutionary biology.

TABLE 1. The biological species concept and some recently proposed
alternatives.

Biological Species Concept

A species is a group of individuals fully fertile inter se, but
barred from interbreeding with other similar groups by its physiological
properties (producing either incompatibility of parents, or sterility of
the hybrids, or both) (Dobzhansky 1935).

Species are groups of actually or potentially interbreeding natural
populations, which are reproductively isolated from other such groups
(Mayr 1942).

Evolutionary Species Concept

A species is a single lineage of ancestral descendant populations or
organisms which maintains its identity from other such lineages and
which has its own evolutionary tendencies and historical fate (Wiley
1978).

Phylogenetic Species Concepts

A phylogenetic species is an irreducible (basal) cluster of organisms
that is diagnosably distinct from other such clusters, and within which
there is a parental pattern of ancestry and descent (Cracraft 1989).

A species is the smallest monophyletic group of common ancestry (de
Queiroz and Donoghue 1990).

Recognition Species Concept

Species are the most inclusive population of individual biparental
organisms which share a common fertilization system (Paterson 1985).

Cohesion Species Concept

A species in the most inclusive population of individuals having the
potential for phenotypic cohesion through intrinsic cohesion mechanisms
(Templeton 1989).

Ecological Species Concept

A species is a lineage (or a closely related set of lineages) which
occupies an adaptive zone minimally different from that of any other
lineage in its range and which evolves separately from all lineages
outside its range (Van Valen 1976).

Internodal Species Concept

Individual organisms are conspecific in virtue of their common
membership of a part of the genealogical network between two
permanent-splitting events or between a permanent split and an
extinction event (Kornet 1993).

ACKNOWLEDGMENTS

My work is supported by a grant from the National Institutes of
Health. I thank A. Berry, J. Bull, D. Futuyma, C. Johnson, M. Leibold,
M. Noor, A. Orr, D. Schemske, M. Turelli, P. Ward, and G. C. Williams
for discussion or comments on the manuscript. I am especially grateful
to Ernst Mayr, whose Animal Species and Evolution inspired me to become
an evolutionary biologist, and whose writings have sustained that
inspiration over the years.

Cracraft, J. 1989. Speciation and its ontology: the empirical
consequences of alternative species concepts for understanding patterns
and processes of differentiation. Pp. 28-59 in Otte and Endler 1989.

Darwin, C. 1859. On the origin of species by means of natural
selection or the preservation of favoured races in the struggle for
life. J. Murray, London.

-----. 1871. The descent of man, and selection in relation to sex. J.
Murray, London.